Hydrobiologia (2012) 685:121–134
DOI 10.1007/s10750-011-0791-4
HABITAT COMPLEXITY
Invasive mussels induce community changes by increasing
habitat complexity
Lyubov E. Burlakova • Alexander Y. Karatayev
Vadim A. Karatayev
•
Received: 1 February 2011 / Accepted: 5 June 2011 / Published online: 2 August 2011
Ó Springer Science+Business Media B.V. 2011
Abstract Habitat complexity is among the most
important factors affecting the diversity, structure, and
density of natural communities. The invasive byssate
bivalves zebra mussel (Dreissena polymorpha (Pallas,
1771)) and golden mussel (Limnoperna fortunei
(Dunker, 1857)) are sessile suspension feeders that
form aggregations (druses), physically changing sediments and increasing habitat complexity, and providing shelter and food for other benthic organisms. In
this study, we explored the impact of the change in
habitat complexity on benthic community created by
druses of L. fortunei and D. polymorpha, formed on
Guest editors: K. E. Kovalenko & S. M. Thomaz /
The importance of habitat complexity in waterscapes
L. E. Burlakova (&) A. Y. Karatayev
Great Lakes Center, Buffalo State College,
1300 Elmwood Ave., Buffalo, NY, USA
e-mail: burlakle@buffalostate.edu
URL: http://www.buffalostate.edu/greatlakescenter/
x732.xml
A. Y. Karatayev
e-mail: karataay@buffalostate.edu
L. E. Burlakova
The Research Foundation of The State University
of New York, Buffalo State College, Office of Sponsored
Programs, 1300 Elmwood Avenue, Buffalo, NY, USA
V. A. Karatayev
University Honors College, State University of New York
at Buffalo, 106 Capen Hall, Buffalo, NY, USA
e-mail: vadimkar@buffalo.edu
various sediments. D. polymorpha was studied in
Europe (Naroch Lake, Belarus) and in North America
(Glen Lake and Lower Nashotah Lake, USA), and
L. fortunei was studied in South America (Rı́o Tercero
Reservoir, Argentina). Druses of D. polymorpha or
L. fortunei and samples of bare nearby sediment
(without druses of exotic mussels) were collected at
each sampling site. We found significant changes in
species richness, density, biomass, taxonomic, and
trophic structure of communities formed in druses
compared to the nearby bare sediments. Community
taxonomic richness increased threefold, and density
increased sevenfold with increasing complexity of
habitat from sand to druse. The feeding functional
group approach indicated that the impact of increased
complexity was reinforced by an increase in food
supply in D. polymorpha and L. fortunei druses. Along
with increasing species richness and densities, byssate
bivalves homogenized benthic communities.
Keywords Invasive species Community effect Habitat complexity Dreissena polymorpha Limnoperna fortunei Taxonomic structure Trophic structure Byssate bivalve
Introduction
Habitat complexity, along with a variety of ecological
processes, has a strong and pervasive influence on
community diversity, structure, and abundance (Bell
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122
et al., 1991; Schluter & Ricklefs, 1993; Rahbek &
Graves, 2001). It has been documented in terrestrial,
freshwater, and marine environments and for both
vertebrate and invertebrate species, that physically
complex habitats contain more species than simple
habitats (Bell et al., 1991). Higher densities in
physically complex habitats may simply be due to
greater living space or surface area. However, the
effects may be more complex, as heterogeneity of the
environment is essential for species co-existence, and
complex habitats offer a variety of different microhabitats and niches, allowing resource partitioning
(Schoener, 1974; Pianka, 1988; Levin, 1992; Downes
et al., 2000). Understanding the mechanisms that
influence benthic community diversity, structure, and
abundance is one of the major goals of aquatic
ecology (Ritchie & Olff, 1999; Almany, 2004;
Taniguchi & Tokeshi, 2004).
The invasive bivalves zebra mussel (Dreissena
polymorpha (Pallas, 1771)) and golden mussel (Limnoperna fortunei (Dunker, 1857)) are sessile suspension feeders that produce byssal threads to form
aggregations (druses) and not only physically change
substrates, increasing habitat complexity for other
benthic organisms, but also affect trophic relationships
and nutrient cycling locally and system-wide via their
filtering activities (Karatayev et al., 1997, 2002, 2010).
Most of the impacts of these invasive mussels in
freshwater systems are a direct result of their functioning as ecosystem engineers (Karatayev et al., 1997,
2002, 2007a, b; Sousa et al., 2009). Ecosystem
engineers are defined as species that ‘‘directly or
indirectly control the availability of resources to other
organisms by causing physical state changes in biotic
or abiotic materials’’ (Jones et al., 1994, 1997). Many
different species have been identified as ecosystem
engineers of aquatic habitats (Flecker, 1996; Wotton
et al., 1998; Statzner et al., 2000), and particularly
bivalves (Dame, 1993, 1996; Ruesink et al., 2005).
The main ecosystem level roles of bivalves include
structural, trophic, and nutrient cycling (Dame, 1996).
Physically, bivalves create three-dimentional structures with their shells and can stabilize sediments
(Gutierrez et al., 2003; Ruesink et al., 2005). Biologically, they affect community structure (both in the
water column and in the benthos), and can influence
community stability, diversity, and interspecies links
(Karatayev et al., 2002). D. polymorpha and L. fortunei have all of the properties of ecosystem engineers
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Hydrobiologia (2012) 685:121–134
(Karatayev et al., 1997, 2002, 2007a, b; Sousa et al.,
2009), and although less information is available on
L. fortunei, we hypothesize that their effect on benthic
community will be similar to that of D. polymorpha.
This knowledge is important, considering that
L. fortunei may colonize many more waterbodies in
central and southern regions of North America than
zebra mussels (Ricciardi, 1998; Karatayev et al.,
2007a, b; Oliveira et al., 2010). Although facilitation
by habitat modifiers in general, and by filter-feeding
bivalves in particular, is a well-known phenomenon,
the effects on the benthic fauna are often modulated
and even reversed by specific species composition
(Afanasiev & Protasov, 1987; Spooner & Vaughn,
2006), suspended sediment concentration (Norkko
et al., 2006), sediment characteristics (Radziejewska
et al., 2009), and geographic location (Buschbaum
et al., 2009).
In this study, we explore the impact of the change
in habitat complexity on the benthic community
created by druses of two exotic byssate bivalves
L. fortunei and D. polymorpha, and investigate how
these impacts vary depending on sediment type. We
hypothesize that druses augment the habitat’s structural complexity and enhance trophic conditions for
associated invertebrates, resulting in large changes in
the benthic community. We assess the impact by
evaluating changes in diversity, density, biomass,
taxonomic composition, and trophic structure of the
community.
Materials and methods
Dreissena polymorpha impact on macroinvertebrates
was studied in Europe and in North America, and
L. fortunei was studied in South America using
previously described methods (Burlakova et al.,
2005; Karatayev et al., 2010). The effect of
D. polymorpha on benthic community was assessed
in Lake Naroch (Republic of Belarus, July 2006), in
Lower Nashotah Lake (Waukesha Co., Wisconsin,
June 2007), and in Glen Lake (Warren Co., New
York, July 2003). The effect of L. fortunei on benthos
was studied in 2006 in Embalse Rı́o Tercero, a
reservoir located in the province of Córdoba, central
Argentina, during a similar season (mid-summer,
December) (Boltovskoy et al., 2009; Karatayev et al.,
Hydrobiologia (2012) 685:121–134
2010). In each lake, samples were collected at one or
more sites. Each sampling site had the same sediment
within a site (e.g., sand). Samples of D. polymorpha
or L. fortunei druses and the same amount of bare
sediment samples not immediately adjacent to the
druse (without druses, ‘‘sediments’’) were collected at
each sampling site. Druses were collected together
with contained sediments and invertebrates (but
without underlying sediments) by a diver, carefully
placed in zip-lock bags, and brought to the surface.
Benthic samples of bare sediments (without druses)
were collected with a tube dredge sampler 7.2 cm in
diameter. All samples were washed through a
500 lm sieve and fixed with 10% buffered formaldehyde. All organisms from all samples were identified to the lowest possible taxonomic level, except
for oligochaetes, where only two species (Stylaria
lacustris (Linnaeus) and Branchiura sowerbyi (Beddard)) were identified, while all others were categorized as Oligochaeta. All organisms were counted,
and weighted after blotting dry on absorbent paper
(total wet weight). Wet biomass was not recorded for
macroinvertebrates collected from Glen Lake. Druse
surface area was estimated as its projection onto a
two-dimensional plane (two-dimensional area of
mussels covering the benthos) and was on average
0.0047 ± 0.0002 m2, n = 54 (mean ± standard
error here and elsewhere unless noted) across all
samples, comparable to the tube sampler catch area
(0.004 m2). Druses and tube samples were approximately similar in total volume, as the height of an
average druse was comparable to the depth of the
tube sample (5–7 cm).
In Glen Lake, nine druses and nine sediment
samples were collected in July 2003 at 1 to 1.5 m
depth from sand (Table 1). In Naroch Lake, we
collected 10 druses and 10 sediment samples from
two sites at 1 m depth each, one site was on bare sand
and another on sand with Chara sp. In the Lower
Nashotah Lake, we collected six D. polymorpha
druses and six samples of bare sediments at three
sites with different sediments: on silt and shells
(2.5 m depth), sand and gravel (1 m depth), and rocks
(1 m depth, rocks incrusted with zebra mussels, vs.
non-incrusted rocks of a similar size). In Rı́o Tercero
Reservoir, we collected 10 samples of L. fortunei
druses and 10 samples of coarse sand with silt at
3.5 m depth (all mussels in \3 m depth were dead
due to the recent drawdown) (Table 1).
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To assign invertebrates found in the benthic
samples to feeding functional groups, we used the
classification suggested by Merritt & Cummins
(1996). For invertebrates that were identified to
species, we used data from Izvekova (1975), Sokolova et al. (1980b), and Monakov (1998, 2003) to
assign the feeding functional group. For invertebrates
identified to genus, we used Merritt and Cummins
(1996) and Thorp & Covich (2001). However, some
species and genera fit into more than one group. For
example, some collectors are known to filter-feed and
gather (e.g., Microtendipes chloris (Meigen, 1818),
Bithynia tentaculata (Linnaeus, 1758), B. leachi
(Scheppard, 1823), Tanytarsus sp.) (Izvekova, 1975;
Merritt & Cummins, 1996; Monakov, 1998). As these
species were abundant in the lakes sampled, we
considered them as ‘‘filtering ? gathering collectors’’, a sub-group within the ‘‘collectors’’ group.
To characterize the convolution of all sampled
substrates, we arranged them in four groups according
to their sediment particle size and increased complexity:
1—sand; 2—silt with shells, and coarse sand with silt;
3—sand with Chara sp., rocks (40–100 mm), and sand
with gravel; 4—druses. Sediment particle size classification has proven to be useful in studies of bivalve
ecology and impacts on benthic communities (Strayer,
1999; Ward & Ricciardi, 2007; Sousa et al., 2007).
Statistical analyses
Macroinvertebrate community structures were assessed
using density, wet biomass, and diversity indices.
PRIMER 6 (Version 6.1.6, Primer E-Ltd. 2006) package
was used to analyze differences in benthic communities.
The sample-to-sample similarity of macroinvertebrate
community composition (density and biomass) was
assessed with the aid of the Bray-Curtis index (BC)
(Bray & Curtis, 1957; Clarke, 1993), based on fourthroot transformed density or biomass data. To visualize
the differences among communities, we used nonmetric multi-dimensional scaling (NMDS), which calculates a set of metric coordinates for samples, most
closely approximating their nonmetric distances
(Legendre & Legendre, 1998). NMDS was found to
be consistently reliable in a comparative study of
ordination methods for community data (Kenkel &
Orlóci, 1986; Clarke, 1993). To test the significance of
differences among communities, we used a non-parametric analogue of ANOVA—analysis of Similarities
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Hydrobiologia (2012) 685:121–134
Table 1 Mean density, wet biomass, taxon richness, and
diversity indices (Margalef’s index of species richness calculated on density data) of benthic communities formed in
Lake, substrate
Mean density (m-2)
S
D
d
Limnoperna fortunei and Dreissena polymorpha druses, and in
nearby bare sediments (number of samples collected from each
substrate, equal to the number of druses, in parentheses)
Mean biomass (g m-2)
Taxa richness
Margalef’s index
S
D
d
S
d
S
D
D
d
Naroch Lake
Sand (10)
3,238
11,355
3.5
4
75
19
9
30
3.3*
1.36
2.54
1.9
Sand and Chara sp. (10)
9,975
19,356
1.9
29
115
4.0
23
20
0.9
2.38
1.93
0.8
Mean
6,606
15,355
2.3
16
95
5.9
25
32
1.3
2.73
3.21
1.2
1,571
27,615
17.6
n.r.
n.r.
n.r.
11
27
2.5*
1.36
2.54
1.9
Glen Lake
Sand (9)
Lower Nashotan
Silt and shells (6)
833
18,165
21.8
3
33
11
9
32
3.6*
1.19
3.16
2.7
10,254
21,764
2.1
7
30
4.3
18
30
1.7*
1.84
2.90
1.6
Sand and gravel (6)
5,708
22,928
4.0
15
26
1.7
20
33
1.7*
2.20
3.19
1.5
Mean
5,599
20,952
17.6
8
30
3.8
30
47
1.6
3.36
4.62
1.4
Rocks (6)
Rio Tercero
Silt and sand (10)
All lakes (57)
4,650
15,313
3.3
9
31
3.5
16
20
1.3*
1.78
1.97
1.1
5,280
19,051
3.6*
11
57
4.9*
64
105
1.6*
7.35
10.55
1.4
Density and biomass of invasive bivalves were excluded from this analysis. Samples were collected in Rı́o Tercero Reservoir,
Argentina (L. fortunei), Lake Naroch (Belarus), Lake Lower Nashotah and Glen Lake (USA) (D. polymorpha). S bare sediment
community, D community in Dreissena/Limnoperna druses, d ratio between druse and sediment community parameters, n.r. not
recorded. For taxa richness and Margalef’s index instead of the mean, total values for the lake are given
* These changes were tested and found significant at P \ 0.001 (2-sided t tests)
(ANOSIM), a resampling technique that uses permutation/randomization methods on BC similarity matrices
to identify differences among groups of samples
(Clarke, 1993). Large values of the test statistic (Global
R) indicate complete separation of groups, and small
values (close to 0) indicate little or no separation. To
decrease the effect of natural differences in species
composition among continents, this analysis was done
on different taxonomic levels including species, genus,
family, order, and class levels.
We used SIMPER (‘‘Similarity Percentage’’) analysis to examine the contribution of each taxon to the
average BC similarity within each druse and sediment communities. To reveal the contribution of
different functional groups to similarity among druse
and sediment communities, we used SIMPER on
density and biomass data by taxa aggregated to
functional feeding groups using the classification
scheme by Merritt & Cummins (1996). Density and
biomass of D. polymorpha and L. fortunei were
excluded from the community for this analysis.
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Univariate diversity indices are used to reduce the
data on the community’s multivariate complexity into
a single index. Different diversity indices emphasize
the species richness (total number of species present
or some adjusted form) or equitability (how evenly
the individuals are distributed among the different
species) components of diversity to varying degrees.
To demonstrate between-sample relationships
obtained from the full range of diversity information
extracted (evenness ? richness) (Clarke & Gorley,
2006) we used PRIMER to create a similarity matrix
of diversity indices (total number of taxa in each
sample, Margalef’s species richness, Pielou’s evenness, Shannon–Wiener diversity index (Log e base),
and Simpson’s diversity index). We applied ANOSIM to this matrix to test for differences in community composition in druses versus bare sediments.
This analysis was then contrasted with the usual
NMDS ordination done on original data (species
density). For all tests, effects were considered
statistically significant at P \ 0.05.
Hydrobiologia (2012) 685:121–134
Results
Changes in diversity, density, and biomass
When we combined all data across three continents,
we found that there were a total of 105 species in all
D. polymorpha and L. fortunei druses, compared to
64 taxa found in all nearby sediments. This increase
in taxa richness was significant for each substrate in
each lake except for sand and Chara sp. in Naroch
Lake (P \ 0.001, 2-sided t tests, Table 1).
The complex 3D structure of druses increased both
density and biomass of associated communities in all
waterbodies studied (Table 1). Excluding density and
biomass of D. polymorpha and L. fortunei, invertebrate densities in druses increased from 1.9 to 22
times and biomass from 1.7 to 19 times, depending
on substrate (Table 1). The effects of druse and
sediment type on the community were both significant (density—druse: R = 0.425, P = 0.001; sediment type: R = 0.466, P = 0.001; biomass—druse:
R = 0.812, P = 0.001; sediment type: R = 0.88,
P = 0.001; two-way ANOSIM). The average density
and biomass of native benthic invertebrates per
sample was significantly higher in druses than in
the sediments (P \ 0.001, t test, Table 1).
When we included D. polymorpha and L. fortunei
into the analysis, we found drastic changes in
community density and biomass. On average, the
mean difference between druses and communities in
nearby bare sediments in density was 10 times (from 5
times in Naroch Lake to 18 in Glen Lake), and in
biomass 994 times (from 624 times in Naroch Lake to
1,281 in Rio Tercero Reservoir) higher in druses than
in bare sediments. Both D. polymorpha and L. fortunei were the dominant species in the druse community.
Taxonomic changes
The presence of D. polymorpha and L. fortunei druses
significantly affected the density and biomass of
benthic communities on all sediments (R = 0.53,
P = 0.001); however, due to natural differences in
species composition among lakes and sediments,
there was a high dissimilarity among benthic communities in different lakes (R = 0.85, P = 0.001,
two-way ANOSIM, Fig. 1A). When the species
matrix was aggregated to the taxonomical level of
genus and higher, the druse community appeared
125
more homogenous, and the changes were better
pronounced (genus level—druse: R = 0.54, lake:
R = 0.76, both P = 0.001; family level—druse:
R = 0.58, lake: R = 0.70, both P = 0.001, Fig. 1B).
We further tested these effects on a dataset
obtained from the full range of diversity information,
using matrix of diversity indices that involve both
species richness and species evenness. With both
dimensions of diversity considered, group separation
was more distinct (2D stress decreased from 0.12 to
0.01, Fig. 2A, B), and the effect of druse was more
important than the difference driven by species
composition in different lakes and substrates (druse:
R = 0.44, P = 0.001, lake: P = 0.39, P = 0.001,
two-way ANOSIM).
Druse and bare sediment communities were dissimilar at 85%, and 20 macroinvertebrate species
contributed each over 2% to the dissimilarity between
the groups (e.g., leach Helobdella stagnalis (Linnaeus,
1758) (4.2%), chironomid Dicrotendipes tritomus
(Kieffer, 1916) (4.1%), gammarid Gammarus lacustris G. O. Sars, 1863 (3.9%). Aggregation of the data to
family level revealed that these differences were due to
higher densities of Chironomidae, Glossiphonidae,
Gammaridae, Caenidae, Asselidae, Planariidae, and
unidentified Oligochaeta in druse communities. In
general, Insecta were responsible for 41% of the
differences between the groups, followed by Malacostraca (19%), Hirudinea (13%), and Gastropoda
(11%); the input of other groups was\10% (Table 2).
Changes in community functional structure
Druse communities were more similar than those
formed on bare sediments when each taxon was
analyzed by its functional feeding mode (Fig. 1C, D;
Table 3). Although gathering collectors and predators
were the most abundant feeding groups in both
communities, they reached higher densities and biomass in the presence of invasive bivalves (Table 3).
Filtering collectors (excluding exotic bivalves), though
having similar densities and biomass in both communities, had a lower relative abundance and thus a lower
contribution to the similarity of druse communities
(Table 3). Scrapers, in contrast, were more abundant in
druse community (Table 3). Gathering collectors,
predators, and scrapers contributed over 80% to the
dissimilarity between druse and sediment communities
(Table 4).
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126
A
B
Hydrobiologia (2012) 685:121–134
2D Stress: 0.12
2D Stress: 0.17
C
D
2D Stress: 0.11
2D Stress: 0.12
Fig. 1 Non-linear MDS plots of benthic samples from Lake
Naroch (Belarus), Lake Lower Nashotah, and Glen Lake
(USA), and Rı́o Tercero Reservoir (Argentina). The samples
were collected in Limnoperna fortunei (Rı́o Tercero Reservoir)
and Dreissena polymorpha (all other lakes) druses (filled
triangles) and in nearby sediments (open circles). The BrayCurtis similarity matrix used for this plot was calculated based
on fourth -root transformed density data for each taxon
indentified in each sample. Densities of L. fortunei and D.
polymorpha were excluded from the community for these
analyses. A data for each species or taxon density (2D stress:
0.12). B species (taxon) density data aggregated to genus level
(2D stress: 0.17). C density of each taxon aggregated by
functional feeding groups according to Merritt & Cummins
(1996) (2D stress: 0.11). D biomass of each taxon aggregated
by functional feeding groups (2D stress: 0.12)
With inclusion of the exotic bivalves (both
D. polymorpha and L. fortunei are filter-feeders), in
all waterbodies druse community was characterized
by extremely high dominance of one functional
feeding group in their trophic structure—filtering
collectors that comprised up to 99% of community’s
wet biomass.
found in druses (13.4 ± 0.6, range 6–22). A significant positive relationship was also found among
habitat complexity and density of invertebrates that
increased over sevenfold from sand to druses
(Fig. 3B).
Macroinvertebrate communities formed in druses
were more similar among themselves than to the
communities in nearby sediments, independently of
where they were formed: similarity of communities in
druses was significantly higher than in bare sediments
(average similarity in sediments: 48.4 ± 7.6, druses:
69.5 ± 2.5, t = -2.64, P = 0.017, one-sided t test)
(Fig. 2B). Consequently, the dissimilarity between
druse communities formed on different sediments in
the same lake was significantly lower than the
dissimilarity between bare sediments in the same lake
Druses increase substrate complexity
and homogenize communities
Taxa richness increased along with the level of
substrate complexity, from 4.1 (±0.4, range: 1–8) on
sand, to 9.9 (±0.5, range 5–15) on more complex
substrates (sand with Chara sp., rocks, and sand with
gravel) (Fig. 3A). The highest taxa richness was
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Hydrobiologia (2012) 685:121–134
127
2D Stress: 0.01
A
B
2D Stress: 0.12
Rio Tercero
Reservoir, Argentina
Lake Lower
Nashotah,
USA
Substrate
druse
sand
sand Chara
silt shells
rock
sand gravel
sand silt
Lake
Naroch,
Belarus
Glen Lake,
USA
Fig. 2 Non-linear MDS ordination plots of benthic macroinvertebrate communities found in samples from Lake Naroch
(Belarus), Lake Lower Nashotah, and Glen Lake (USA), and
Rı́o Tercero Reservoir (Argentina). The samples were collected
in Limnoperna fortunei (Rı́o Tercero Reservoir) or Dreissena
polymorpha (all other lakes) druses, and in nearby sediments.
Densities of L. fortunei and D. polymorpha were excluded from
the community for these analyses. A NMDS ordination of
similarity indices of the benthic community (taxon densities)
based on normalized Euclidian distances of diversity indices of
all samples. Filled triangles L. fortunei or D. polymorpha
druses; open circles sediments. Diversity indices used were:
total number of species in each sample, Margalef’s species
richness; Pielou’s evenness, Shannon–Wiener diversity index
(log e), and Simpson’s index. B NMDS ordination of benthic
macroinvertebrate communities found in L. fortunei or D.
polymorpha druses and in nearby sediments. The Bray-Curtis
similarity matrix used for this plot was calculated based on
fourth-root transformed density data for each taxon indentified
in each sample. Reversed open triangles silt and shells; open
circles sand and silt; grey filled circles sand; stars sand with
Chara sp.; grey diamonds sand and gravel; grey squares rocks;
filled triangles L. fortunei or D. polymorpha druses. Samples
from different lakes are indicated by shapes
(average dissimilarity in bare sediment: 77.4 ± 6.6,
druse: 35.9 ± 4.3, t = -5.13, P = 0.0018, one-sided
t test).
Discussion
We found large changes in species richness, density,
biomass, taxonomic, and trophic structure of communities formed in byssate mussel aggregations compared to the nearby sediments. The mechanism of
these changes is complex, but can be roughly divided
into two main categories: structural and trophic.
Structural changes (physical alteration of the
sediment) include increase in surface area due to
sheer addition of bivalve shells, which serve as a
substrate for the attachment of a variety of sessile
organisms (e.g., algae, sponges, insect larvae, etc.),
including the bivalves themselves. In addition, this
complex two- and three-dimensional structure formed
by the shells attached to each other with byssal
threads provides the habitat heterogeneity and complexity in the form of interstices between living and
dead shells, and cavities in empty shells from dead
mussels. Empty shells do not decompose or dissolve
readily in lakes but accumulate on the bottom,
creating reef-like structures which provide additional
hard-substratum habitat (Karatayev et al., 2002).
These reefs made of live mussels and spent shells
are used by various invertebrates (e.g. Gammaridae,
Trichoptera, etc.) as refuges from predation and from
physical (e.g., waves, currents) or physiological
stresses (e.g., temperature, desiccation, lack of oxygen) (reviewed in Karatayev et al., 1997, 2002;
Stewart et al., 1998a; Gutierrez et al., 2003). It has
been shown that dreissenid aggregations create
habitat for species that would otherwise be infrequent
or absent in the environment, providing them with
reliable shelter, and thus reducing the foraging
success of predators (Botts & Patterson, 1996;
Stewart et al., 1998b, 1999; Mayer et al., 2001; Cobb
& Watzin, 2002; Beekey et al., 2004).
Community changes resulting from increased
complexity of habitat have been seen in other
environments. Surface roughness affects flow
micro-environments and the ability of fauna to cling
to stones (Lancaster & Mole, 1999), alters competitive outcomes (e.g., Fletcher & Underwood, 1987),
or the local success of predators (e.g., Fairweather,
1988; Robson, 1996). Moreover, it has been demonstrated that patch size and structural complexity have
independent effects on macroinvertebrate assemblages, suggesting that the relationship between the
number of species and surface area is not a sampling
123
128
Table 2 Results of
multivariate SIMPER
(‘‘Similarity Percentages—
species contributions’’)
analyses on benthic
macroinvertebrate taxa in
Dreissena polymorpha and
Limnoperna fortunei druse
communities (druse) and in
communities in nearby
sediments (sediment)
Original data on species
(and in some cases higher
taxa) densities was
aggregated to order and
class level to decrease the
natural differences in
species composition among
continents. Average density
(fourth-root transformed),
taxon contribution to the
dissimilarity between druse
and sediment communities
(%), and cumulative
contribution to the
dissimilarity are given by
taxa
a
Only two species of
oligochaetes (Stylaria
lacustris and Branchiura
sowerbyi) were identified to
species; all others were
categorized as oligochaetes
Hydrobiologia (2012) 685:121–134
Taxa
Druse average
density
Contribution
(%)
Cumulative
contribution (%)
By Order (average dissimilarity = 60.0%)
Diptera
25.91
17.34
26.29
26.29
7.16
6.26
1.83
2.07
10.61
9.87
36.9
46.77
Basommatophora
5.69
0.73
8.46
55.23
Ephemeroptera
5.71
2.5
7.85
63.08
Trichoptera
3.96
0.61
6.58
69.66
Isopoda
3.52
0.45
6.44
76.11
Tricladida
3.3
0.22
5.16
81.27
Oligochaetaa
3.3
3.77
5.07
86.34
Haplotaxida
2.16
1.02
4.3
90.64
Arhynchobdellida
1.11
0.36
2.29
92.93
Veneroida
0.38
0.77
1.58
94.51
Amphipoda
Rhynchobdellida
Neotaenioglossa
0.86
0.08
1.43
95.94
Megaloptera
0.68
0.14
1.14
97.08
Odonata
0.83
0.00
1.09
98.17
Coleoptera
0.44
0.07
0.67
98.84
Decapoda
0.28
0.00
0.56
99.4
Tubificida
Architaenioglossa
0.00
0.12
0.14
0.00
0.28
0.21
99.68
99.89
Hemiptera
0.00
0.07
0.11
100
By Class (average dissimilarity = 54.5%)
Insecta
37.53
20.74
41.18
41.18
Malacostraca
10.96
2.28
18.72
59.90
Hirudinea
7.37
2.44
12.78
72.67
Gastropoda
6.66
0.82
10.98
83.66
Oligochaeta
5.46
4.93
8.90
92.55
Turbellaria
3.30
0.22
5.70
98.26
Bivalvia
0.38
0.77
1.74
100.00
artifact due to more complex habitats having larger
areas, and therefore sampling more individuals
(Matias et al., 2010). In aggregations of byssate
epifaunal bivalves the effect of increased habitat
complexity is reinforced by trophic changes in the
habitat. These filter-feeding bivalves greatly enhance
the rates of deposition of both organic and inorganic
material on the bottom, increasing sedimentation
rates by several orders of magnitude. Filtered particles are sorted, and either consumed, or rejected.
Rejected particles are bound in mucus, expelled as
pseudofeces, and deposited onto the bottom. This
results in greatly increased organic content of sediments, and provides an enhanced food subsidy for
benthic deposit feeders (Karatayev et al., 1983, 1994,
123
Sediment average
density
2002, 2007a, b; Karatayev & Burlakova, 1992, 1995;
Botts & Patterson, 1996; Stewart et al., 1998a).
Another source of food for benthic invertebrates
inhabiting druses is the algal and bacterial communities flourishing on bivalve shells and in their aggregations. Over 150 algae species, mostly belonging to
Bacillariophyta and Chlorophyta, were identified in
periphyton samples collected from D. polymorpha
shells in Lake Naroch, Belarus (Makarevich et al.,
2008). The total area of hard substrate presented by
D. polymorpha shells in Lake Naroch is equal to 11%
of the lake surface area (Makarevich et al., 2008).
D. polymorpha clusters were shown to increase heterotrophic bacterial density, induce changes in community structure, and enhance bacterial activity and
Hydrobiologia (2012) 685:121–134
129
Table 3 Results of multivariate SIMPER (‘‘Similarity Percentages—species contributions’’) analyses on benthic macroinvertebrate taxa in Dreissena polymorpha and Limnoperna
Functional feeding group
Average
density
fortunei druse communities (druse) and in communities in
nearby sediments (sediment)
Average
biomass
Contribution by
density (%)
Contribution by
biomass (%)
Sediment community (average similarity by density = 53.7; by biomass = 52.0)
Gathering collectors
17.87
3.25
71.14
68.73
Predators
8.03
1.64
22.53
24.18
Shredders
1.68
0.22
2.27
1.63
Filtering collectors
1.86
0.34
1.99
2.09
Filtering gathering collectors
1.55
0.35
1.53
2.37
0.53
1.00
Scrapers
1.21
0.34
Druse community (average similarity by density = 74.3; by biomass = 72.7)
Gathering Collectors
40.01
7.18
62.57
58.29
Predators
18.13
4.42
27.49
29.82
Scrapers
5.26
1.18
4.48
5.03
Filtering gathering collectors
3.89
0.96
2.95
4.09
Shredders
2.61
0.50
1.42
1.37
Filtering collectors
1.76
0.41
1.08
1.40
Original density and biomass data were aggregated by functional feeding groups according to (Merritt & Cummins, 1996). Average
taxa density and biomass (fourth-root transformed), contribution to the Bray-Curtis similarity to the community (%), and cumulative
contribution to the similarity are given by each group. Density and biomass of invasive bivalves were excluded from this analysis
Table 4 Results of multivariate SIMPER analyses on benthic macroinvertebrate taxa in Dreissena polymorpha and Limnoperna
fortunei druse communities (druse) and in communities in nearby sediments (sediment)
Functional feeding group
Sediment
average
Druse
average
Contribution
(%)
Cumulative
contribution (%)
Density (average dissimilarity = 49.8)
Gathering collectors
17.87
40.01
47.51
Predators
8.03
18.13
24.94
47.51
72.45
Scarpers
1.21
5.26
9.50
81.95
Filtering gathering collectors
1.55
3.89
7.34
89.29
Shredders
1.68
2.61
5.45
94.74
Filtering collectors
1.86
1.76
5.26
100.00
Gathering collectors
3.25
7.18
40.71
40.71
Predators
1.64
4.42
30.18
70.88
Scarpers
Filtering gathering collectors
0.34
0.35
1.18
0.96
10.67
8.52
81.55
90.07
Biomass (average dissimilarity = 51.5)
Filtering collectors
0.34
0.41
5.22
95.29
Shredders
0.22
0.50
4.71
100.00
Original density and biomass data were aggregated by functional feeding groups according to (Merritt & Cummins, 1996). Average
taxa density and biomass (fourth-root transformed), contribution to the Bray-Curtis dissimilarity between druse and sediment
communities (%), and cumulative contribution to the dissimilarity are given by each group. Density and biomass of invasive bivalves
were excluded from this analysis
123
130
Hydrobiologia (2012) 685:121–134
A 24
22
20
y = -0.45 + 3.43x;
r = 0.73, P < 0.001, r2 = 0.53
Taxa richness
18
16
14
12
10
8
6
4
2
0
1
2
3
4
Complexity index
Log Total Sample Density m-2
B
11
y = 6.50 + 0.81*x; r = 0.81, P < 0.001; r2 = 0.66
10
9
8
7
6
5
1
2
3
4
Complexity index
Fig. 3 Relationship between macroinvertebrate taxa richness
(A) and log-transformed total density (B) in each sample, and
the degree of habitat complexity expressed in increasing order
from sand (1), to silt with shells, or coarse sand with silt (2),
sand with Chara sp., rocks, and sand and gravel (3). Druses on
all sediments were given a complexity index of 4. The line
represents linear regression with 95% confidence bands,
regression equation is given on each graph
metabolic diversity compared to bare sediments
(Lohner et al., 2007). Microbial community in druses
can mineralize a significant portion of the nutrients
contained in the D. polymorpha feces and pseudofeces, increasing bioavailable nutrients and altering
nutrient cycling and nutrient concentrations in and
near D. polymorpha druses (Lohner et al., 2007). In
addition, aggregations of bivalve shells alter water
flow and infiltration into sediments, affecting the
transport of particles and solutes (Dame, 1996; Gutierrez et al., 2003). Due to structural and trophic
complexity, the druse community was the richest, both
in terms of diversity and density (Table 1; Fig. 3).
The intricate nature of habitat complexity, i.e., the
interplay of structural and trophic components that
123
enhance taxonomic and numerical richness, has been
demonstrated in other environments (e.g., Bell et al.,
1991; Schluter & Ricklefs, 1993; Rahbek & Graves,
2001). More complex substrates often have higher
trophic values, e.g., plants recolonize rough substrates
more quickly that smooth surfaces (Downes et al.,
2000). Sand with Chara in Lake Naroch attracted
more animals compared to bare sand not only due to
the larger area and structural complexity provided by
Chara, but also due to an additional food source—
periphyton growing on Chara. Downes et al. (2000)
showed experimentally that both surface texture and
macroalgae increase species richness of stream invertebrates independently of each other, and both sources
of structure are important during colonization.
Increase in habitat complexity due to aggregations
of exotic byssate bivalves, coupled with organic
enrichment, induced profound changes in community
diversity, taxonomic and trophic structure, and interspecies links. Often, community changes induced by
increased habitat complexity are revealed by either
increased species richness or density, and to date
there are few studies of resultant changes in the
trophic structure of communities (Lvova-Kachanova
& Izvekova, 1978; Sokolova et al., 1980a; Karatayev
& Burlakova, 1992; Burlakova et al., 2005; Ward &
Ricciardi, 2007). The feeding functional group
approach enables a quantitative assessment of the
degree of dependence of the invertebrate biota on
particular food resources (Merritt & Cummins, 1996).
This approach is also a key to understanding the
taxonomical changes in a community as a result of
changes in their habitat.
We found a dramatic shift in the benthic trophic
structure in both D. polymorpha and L. fortunei
aggregations. The structure of feeding functional
groups in the new community, including invasive
bivalves, was overwhelmingly dominated by collectors-filterers. Both D. polymorpha and L. fortunei were
the dominant benthic species in terms of biomass.
Feces and pseudofeces, organic matter deposited
actively and passively, and the phyto-, zooperiphyton
and bacteria thriving on shells provide food for
collectors and scrapers, which increased in density
(Table 3), explaining the dominance of isopods, amphipods, gastropods, mayflies, and some trichopterans,
oligochaetes, and chironomids (Table 2). All these
animals are characteristic of druse communities
(Sokolova et al., 1980a; Karatayev & Lyakhnovich,
Hydrobiologia (2012) 685:121–134
1990; Karatayev & Burlakova, 1992; Botts & Patterson, 1996; Ricciardi et al., 1997; Stewart et al., 1998a;
Karatayev et al., 2002; Ward & Ricciardi, 2007).
Abundance of food and shelter in druses also
attracted predators, explaining the higher densities of
leeches, dragonflies, and Megaloptera in druses
compared to bare sediments nearby. Similar changes
were found in D. polymorpha aggregations in both
Europe and North America (reviewed in Karatayev
et al., 1983, 1997, 2002, 2007a; Ward & Ricciardi,
2007). Small-grain sediments such as sand were
dominated by small animals that live within the
sediment (e.g., chironomids and oligochaetes), while
the druse community was composed of larger animals
(snails, amphipods, isopods, trichopterans, and
leeches). This explains the almost threefold increase
in biomass of druse communities (without consideration of the biomass of exotic bivalves, Table 1).
Druses of D. polymorpha and L. fortunei, including
the exotic bivalves themselves, increased local densities by a factor of ten, and biomass—by a factor of a
thousand, and both bivalves dominated the resulting
community in terms of the density and biomass.
In agreement with our hypothesis, we found that
the mechanism by which L. fortunei affects benthic
assemblages was the same as that of D. polymorpha,
both in terms of species richness and density of
benthic macroinvertebrates (Table 1). Although the
effects on the benthic fauna were modulated by
distinct species assemblages in different substrates,
lakes, and continents, when we aggregated the
species matrix to higher taxonomical levels, the
druse community appeared more homogenous than
the communities in bare sediments nearby, independently of which bivalve was forming the druse. Thus,
we further hypothesize that similar trophic and
taxonomic community changes should be expected
as a result of the introduction of other freshwater or
marine epifaunal byssal bivalves.
Druse inhabitants are predominantly epifaunal
organisms which are likely to take advantage of both
the resources and structural complexity provided by
druses. Infaunal invertebrates (e.g., burrowing oligochaetes, mayflies) may avoid druses. As a result,
species dominant in bare substrates often were not
found in druses nearby (e.g., burrowing oligochaete
B. sowerbyi in Rio Tercero and burrowing mayfly
Hexagenia sp. in Lake Lower Nashotah). Epifaunal
organisms are also highly mobile and may rapidly
131
colonize druses on soft sediments (Mörtl & Rothhaupt, 2003), while many infaunal species are less
mobile (Merritt et al., 1984).
Due to the variety of sampled substrates (e.g.,
sand, sand and Chara, rocks, silt and shells, druses
etc.), we used a categorical measure of habitat
convolution based on substrate particle size and
complexity. While this measure demonstrated the
increase in both diversity and species richness with
increasing habitat complexity, a uniform index
describing both area and structural complexity (e.g.,
refuge space, fractural dimension, Kostylev et al.,
2005; Warfe et al., 2008) will be very useful for
further studies that involve comparing habitats very
different in nature.
We found a large increase in both species’ diversity
and density with increasing habitat complexity from
sand to druses (Table 1, Fig. 3). The largest similarity
was found among communities formed on druses on
rocks, and druses on sand and gravel (Fig. 2B). The
druse communities, independently of the substrate
where the druses were found, included organisms
more typical of rocky substrata, such as gammarid
amphipod and isopod crustaceans, hydroids, flatworms, leeches, and snails (Karatayev et al., 1997,
2002, 2007b; Bially & Macisaac, 2000; Beekey et al.,
2004; Ward & Ricciardi, 2007). Likewise, in marine
sedimentary environments, epifauna normally unable
to occupy soft sediments are restricted in their
occurrence to the mussel bed (Dittmann, 1990;
Robinson & Griffiths, 2002). The most dissimilar
were druse communities from communities formed in
soft sediments (e.g., sand, Fig. 2B).
Macroinvertebrate communities formed in druses
were more similar among themselves than to the
communities in nearby sediments, independently of
where they were formed (Fig. 2B). In addition, they
were less dissimilar among themselves than communities formed on bare substrates in the same lake.
Therefore, along with increasing species richness and
densities, both bivalves homogenize freshwater benthic
communities, making them more similar independently
of which substrate or part of the lake they colonize.
Conclusions
We found significant changes in species richness,
density, biomass, taxonomic, and trophic structure of
123
132
communities formed in druses of D. polymorpha and
L. fortunei compared to the nearby bare sediments.
The feeding functional group approach allowed us to
understand the taxonomical changes in community as
a result of habitat change, and indicated that the
effect of increased habitat complexity in druses was
reinforced by increased food availability. We found a
threefold increase in community taxonomic richness
and a sevenfold increase in density with increasing
complexity of habitat from sand to druse. Along with
increasing species richness and densities, both
bivalves also homogenized freshwater benthic communities, making them more similar independently of
which substrate or part of the lake they colonized.
Acknowledgments The research was partly supported by
grant number 45613 from Wisconsin Department of Natural
Resources and University of Wisconsin at Madison. We are
thankful to Dr. Demetrio Boltovskoy (Universidad de Buenos
Aires, Argentina) for field support in Argentina. We appreciate
the help of the Director of the Naroch Biological Station
(Belarusian State University) Dr. T. V. Zhukova, and the staff
of the Station for assistance in the field in Belarus. We are
thankful to Rhonda Mood for identification of Glen Lake
samples. We would like to thank Richard C. Lathrop and Heidi
Bunk (Wisconsin Department of Natural Resources), James F.
Kitchell, M. Jake Vander Zanden, and other faculty and staff of
the Center for Limnology (University of Wisconsin-Madison)
for providing space, lab and field support in Wisconsin, and
Denise Mayer (New York State Museum Field Research
Laboratory) for field assistance in New York. Research
Foundation of SUNY provided support for LEB during
manuscript preparation.
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